Curcumin induces apoptosis in human gastric carcinoma AGS cells and colon carcinoma HT-29 cells through mitochondrial dysfunction and endoplasmic reticulum stress

Apoptosis

Volumn 18, Issue 11, 2013, Pages 1391-1402

  Cao, Aili ^a   Li, Qi ^a   Yin, Peihao ^a   Dong, Yang ^a   Shi, Hailian ^a   Wang, Li ^a   Ji, Guang ^a   Xie, Jianqun ^a   Wu, Dazheng ^a  

^a SHANGHAI UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

Author keywords

Apoptosis; Curcumin; Endoplasmic reticulum stress; Mitochondrial function

Indexed keywords

2 AMINOETHOXYDIPHENYLBORANE; ADENOSINE TRIPHOSPHATASE; CALCIUM; CARBONYL CYANIDE CHLOROPHENYLHYDRAZONE; CCAAT ENHANCER BINDING PROTEIN; CCAAT ENHANCER BINDING PROTEIN HOMOLOGOUS PROTEIN; CURCUMIN; DEATH RECEPTOR; FAS ASSOCIATED DEATH DOMAIN PROTEIN; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; LIPOCORTIN 5; PHOSPHATIDYLSERINE; PROCASPASE 3; PROCASPASE 7; PROCASPASE 8; PROCASPASE 9; PROPIDIUM IODIDE; PROTEIN BAX; PROTEIN BCL 2; SERCA2ATPASE; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; COLON CARCINOMA; CONTROLLED STUDY; CURCUMA LONGA; CYTOSOL; DOWN REGULATION; DRUG CYTOTOXICITY; DRUG MECHANISM; ENDOPLASMIC RETICULUM STRESS; ENZYME PHOSPHORYLATION; ENZYME RELEASE; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; UPREGULATION;

CURCUMA LONGA;

ANNEXIN A5; ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; CALCIUM; CASPASES; CELL LINE, TUMOR; CELL PROLIFERATION; COLORING AGENTS; CURCUMA; CURCUMIN; ENDOPLASMIC RETICULUM STRESS; FAS-ASSOCIATED DEATH DOMAIN PROTEIN; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MAP KINASE KINASE 4; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; PLANT EXTRACTS; RNA, SMALL INTERFERING; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR CHOP;

EID: 84886422014     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-013-0871-1     Document Type: Article

References (45)

1. Hengartner MO (2000) The biochemistry of apoptosis. Nature 407(6805):770-776
2. Grimm S, Brdiczka D (2007) The permeability transition pore in cell death. Apoptosis 12(5):841-855
3. Gorman AM, Healy SJ, Jager R, Samali A (2012) Stress management at the ER: regulators of ER stress-induced apoptosis. Pharmacol Ther 134(3):306-316. doi: 10.1016/j.pharmthera.2012.02.003
4. Wu Y, Fabritius M, Ip C (2009) Chemotherapeutic sensitization by endoplasmic reticulum stress: increasing the efficacy of taxane against prostate cancer. Cancer Biol Ther 8(2):146-152
5. Oyadomari S, Mori M (2004) Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 11(4):381-389
6. Luciani DS, Gwiazda KS, Yang TL, Kalynyak TB, Bychkivska Y, Frey MH, Jeffrey KD, Sampaio AV, Underhill TM, Johnson JD (2009) Roles of IP3R and RyR Ca2+ channels in endoplasmic reticulum stress and beta-cell death. Diabetes 58(2):422-432. doi: 10.2337/db07-1762
7. Belakavadi M, Salimath BP (2005) Mechanism of inhibition of ascites tumor growth in mice by curcumin is mediated by NF-kB and caspase activated DNase. Mol Cell Biochem 273(1-2):57-67
8. Weir NM, Selvendiran K, Kutala VK, Tong L, Vishwanath S, Rajaram M, Tridandapani S, Anant S, Kuppusamy P (2007) Curcumin induces G2/M arrest and apoptosis in cisplatin-resistant human ovarian cancer cells by modulating Akt and p38 MAPK. Cancer Biol Ther 6(2):178-184
9. Pongrakhananon V, Nimmannit U, Luanpitpong S, Rojanasakul Y, Chanvorachote P (2010) Curcumin sensitizes non-small cell lung cancer cell anoikis through reactive oxygen species-mediated Bcl-2 downregulation. Apoptosis 15(5):574-585. doi: 10.1007/s10495-010-0461-4
10. Javvadi P, Segan AT, Tuttle SW, Koumenis C (2008) The chemopreventive agent curcumin is a potent radiosensitizer of human cervical tumor cells via increased reactive oxygen species production and overactivation of the mitogen-activated protein kinase pathway. Mol Pharmacol 73(5):1491-1501. doi: 10.1124/mol.107.043554
11. Bhaumik S, Anjum R, Rangaraj N, Pardhasaradhi BV, Khar A (1999) Curcumin mediated apoptosis in AK-5 tumor cells involves the production of reactive oxygen intermediates. FEBS Lett 456(2):311-314
12. Thayyullathil F, Chathoth S, Hago A, Patel M, Galadari S (2008) Rapid reactive oxygen species (ROS) generation induced by curcumin leads to caspase-dependent and -independent apoptosis in L929 cells. Free Radic Biol Med 45(10):1403-1412. doi: 10.1016/j.freeradbiomed.2008.08.014
13. Jaiswal AS, Marlow BP, Gupta N, Narayan S (2002) Beta-catenin-mediated transactivation and cell-cell adhesion pathways are important in curcumin (diferuylmethane)-induced growth arrest and apoptosis in colon cancer cells. Oncogene 21(55):8414-8427
14. Jung EM, Lim JH, Lee TJ, Park JW, Choi KS, Kwon TK (2005) Curcumin sensitizes tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-induced apoptosis through reactive oxygen species-mediated upregulation of death receptor 5 (DR5). Carcinogenesis 26(11):1905-1913
15. Wang M, Ruan Y, Chen Q, Li S, Wang Q, Cai J (2011) Curcumin induced HepG2 cell apoptosis-associated mitochondrial membrane potential and intracellular free Ca2+ concentration. Eur J Pharmacol 650(1):41-47. doi: 10.1016/j.ejphar. 2010.09.049
16. Logan-Smith MJ, Lockyer PJ, East JM, Lee AG (2001) Curcumin, a molecule that inhibits the Ca2+-ATPase of sarcoplasmic reticulum but increases the rate of accumulation of Ca2+. J Biol Chem 276(50):46905-46911
17. Bilmen JG, Khan SZ, Javed MH, Michelangeli F (2001) Inhibition of the SERCA Ca2+ pumps by curcumin. Curcumin putatively stabilizes the interaction between the nucleotide-binding and phosphorylation domains in the absence of ATP. Eur J Biochem 268(23):6318-6327
18. Sumbilla C, Lewis D, Hammerschmidt T, Inesi G (2002) The slippage of the Ca2+ pump and its control by anions and curcumin in skeletal and cardiac sarcoplasmic reticulum. J Biol Chem 277(16):13900-13906
19. Yang J, Wu LJ, Tashiro S, Onodera S, Ikejima T (2008) Nitric oxide activated by p38 and NF-kappaB facilitates apoptosis and cell cycle arrest under oxidative stress in evodiamine-treated human melanoma A375-S2 cells. Free Radic Res 42(1):1-11. doi: 10.1080/10715760701762407
20. Ferreiro E, Costa R, Marques S, Cardoso SM, Oliveira CR, Pereira CM (2008) Involvement of mitochondria in endoplasmic reticulum stress-induced apoptotic cell death pathway triggered by the prion peptide PrP(106-126). J Neurochem 104(3):766-776
21. Fernandez SF, Huang MH, Davidson BA, Knight PR 3rd, Izzo JL Jr (2005) Mechanisms of angiotensin II-mediated decreases in intraneuronal Ca2+ in calcium-loaded stellate ganglion neurons. Hypertension 45(2):276-282
22. Limke TL, Otero-Montanez JK, Atchison WD (2003) Evidence for interactions between intracellular calcium stores during methylmercury-induced intracellular calcium dysregulation in rat cerebellar granule neurons. J Pharmacol Exp Ther 304(3):949-958
23. Wu Y, Zhang H, Dong Y, Park YM, Ip C (2005) Endoplasmic reticulum stress signal mediators are targets of selenium action. Cancer Res 65:9073-9079
24. Misra UK, Pizzo SV (2010) Modulation of the unfolded protein response in prostate cancer cells by antibody-directed against the carboxyl-terminal domain of GRP78. Apoptosis 15(2):173-182. doi: 10.1007/s10495-009-0430-y
25. Strimpakos AS, Sharma RA (2008) Curcumin: preventive and therapeutic properties in laboratory studies and clinical trials. Antioxid Redox Signal 10(3):511-545. doi: 10.1089/ars.2007.1769
26. Eigner D, Scholz D (1999) Ferula asa-foetida and Curcuma longa in traditional medical treatment and diet in Nepal. J Ethnopharmacol 67:1-6
27. Sharma RA, Euden SA, Platton SL et al (2004) Phase I clinical trial of oral curcumin: biomarkers of systemic activity and compliance. Clin Cancer Res 10:6847-6854
28. Fang M, Jin Y, Bao W et al (2012) In vitro characterization and in vivo evaluation of nanostructured lipid curcumin carriers for intragastric administration. Int J Nanomedicine 7:5395-5404
29. Lin HH, Huang HP, Huang CC, Chen JH, Wang CJ (2005) Hibiscus polyphenol-rich extract induces apoptosis in human gastric carcinoma cells via p53 phosphorylation and p38 MAPK/FasL cascade pathway. Mol Carcinog 43:86-99
30. Oz HS, Ebersole JL (2010) Green tea polyphenols mediated apoptosis in intestinal epithelial cells by a Fadd-Dependent Pathway. J Cancer Ther 1:105-113
31. Rauert H, Stuhmer T, Bargou R, Wajant H, Siegmund D (2011) TNFR1 and TNFR2 regulate the extrinsic apoptotic pathway in myeloma cells by multiple mechanisms. Cell Death Dis 2:e194
32. Viswanath V, Wu Y, Boonplueang R, Chen S, Stevenson FF, Yantiri F, Yang L, Beal MF, Andersen JK (2001) Caspase-9 activation results in downstream caspase-8 activation and bid cleavage in 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine-induced Parkinson's disease. J Neurosci 21(24):9519-9528
33. Li H, Zhu H, Xu CJ, Yuan J (1998) Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94(4):491-501
34. Zheng HC, Sun JM, Wei ZL, Yang XF, Zhang YC, Xin Y (2003) Expression of Fas ligand and caspase-3 contributes to formation of immune escape in gastric cancer. World J Gastroenterol 9(7):1415-1420
35. Bennett MW, O'Connell J, O'Sullivan GC, Roche D, Brady C, Kelly J, Collins JK, Shanahan F (1999) Expression of Fas ligand by human gastric adenocarcinomas: a potential mechanism of immune escape in stomach cancer. Gut 44(2):156-162
36. Bakhshi J, Weinstein L, Poksay KS, Nishinaga B, Bredesen DE, Rao RV (2008) Coupling endoplasmic reticulum stress to the cell death program in mouse melanoma cells: effect of curcumin. Apoptosis 13(7):904-914. doi: 10.1007/s10495-008-0221-x
37. Binet F, Chiasson S, Girard D (2010) Evidence that endoplasmic reticulum (ER) stress and caspase-4 activation occur in human neutrophils. Biochem Biophys Res Commun 391(1):18-23. doi: 10.1016/j.bbrc.2009.10.141
38. Esther AO, Lawrence HB (2005) Caspase-12 and caspase-4 are not required for caspase-dependent endoplasmic reticulum stress-induced apoptosis. J Biol Chem 280:29578-29597
39. McCullough KD, Martindale JL, Klotz LO, Aw TY, Holbrook NJ (2001) Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol Cell Biol 21(4):1249-1259
40. Sanchez AM, Martinez-Botas J, Malagarie-Cazenave S, Olea N, Vara D, Lasuncion MA, Diaz-Laviada I (2008) Induction of the endoplasmic reticulum stress protein GADD153/CHOP by capsaicin in prostate PC-3 cells: a microarray study. Biochem Biophys Res Commun 372(4):785-791. doi: 10.1016/j.bbrc.2008.05. 138
41. Liu H, Qian J, Wang F, Sun X, Xu X, Xu W, Zhang X (2010) Expression of two endoplasmic reticulum stress markers, GRP78 and GADD153, in rat retinal detachment model and its implication. Eye (Lond) 24(1):137-144. doi: 10.1038/eye.2009.20
42. Park MT, Song MJ, Lee H, Oh ET, Choi BH, Jeong SY, Choi EK, Park HJ (2011) Beta-lapachone significantly increases the effect of ionizing radiation to cause mitochondrial apoptosis via JNK activation in cancer cells. PLoS ONE 6(10):e25976. doi: 10.1371/journal.pone.0025976
43. 2+-ATPase (SERCA). PLoS ONE 7(2):e31905. doi: 10.1371/journal.pone.0031905
44. 2+ depletion and cytochrome c release. Biochem Biophys Res Commun 303(4):1073-1079
45. 2+ concentration within the endoplasmic reticulum. Proc Natl Acad Sci USA 97(11):5723-5728